Agriculture, Ecosystems and Environment 185 (2014) 106–117

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Agriculture, Ecosystems and Environment

journal homepage: www.elsevier.com/locate/agee

Soil ecosystem services and land use in the rapidly changing Orinoco
River Basin of Colombia
Patrick Lavelle a,b,∗ , Nubia Rodríguez c , Orlando Arguello c , Jaime Bernal c , Cesar Botero a ,
Paula Chaparro a , Yolanda Gómez c , Albert Gutiérrez c , María del Pilar Hurtado a ,
Sandra Loaiza a , Sandra Xiomara Pullido c , Edgar Rodríguez a , Catalina Sanabria a ,
Elena Velásquez d , Steven J. Fonte a,1
a
Institut de Recherche pour le Développement, BIOEMCO, 32 rue H. Varagnat, 93143 BONDY Cedex, France
b
Centro Internacional de Agricultura Tropical, AA 6713 Cali, Colombia
c
Corporación Colombiana de Investigacion Agropecuaria, Centro de La Libertad, Villavicencio, Meta, Colombia
d
Universidad Nacional de Colombia, Palmira, Valle, Colombia

a r t i c l e i n f o a b s t r a c t

Article history: In the Orinoco River Basin of eastern Colombia large scale and rapid conversion of natural savannas
Received 12 March 2013 into commercial agriculture exists as a critical threat for the ecological integrity of this fragile region.
Received in revised form The highly acidic and compacted soils inherent to this region require thorough physical and chemical
16 December 2013
conditioning in order for intensive cropping systems to be established. Assessing the impact of this dra-
Accepted 20 December 2013
matic soil perturbation on biodiversity, ecosystem services and other elements of the natural capital is
an urgent task for designing sustainable management options in the region. To address this need, we
Keywords:
evaluated soil macro invertebrate communities and soil-based ecosystem services (climate regulation,
Agricultural intensification
Ecosystem function
hydrologic functions, soil stability provided by macro aggregation and nutrient provision potential) in
Llanos Orientales four major production systems: improved pastures, annual crops (rice, corn and soy bean), oil palm and
Soil macro fauna rubber plantations, and compared them to the original savanna. Fifteen plots of each system were sam-
Soil quality pled along a 200 km natural gradient of soil and climatic conditions. In each plot, we assessed climate
regulation by measuring green house gas emissions (N2 O, CH4 and CO2 ) and C storage in aboveground
plant biomass and soil (0–20 cm). Soil biodiversity (macro invertebrate communities) and three other
soil-based ecosystem services, were assessed using sets of 12–20 relevant variables associated with each
service and synthesized via multivariate analyses into a single indicator for each ecosystem function,
adjusted in a range of 0.1–1.0. Savannas yielded intermediate values for most indicators, while each
production system appeared to improve at least one ecosystem service. For example, nutrient provision
(chemical fertility) was highest in annual cropping systems (0.78 ± 0.03) due to relatively high con-
centrations of Ca, Mg, N, K, and available P and low Al saturation. Hydrological functions and climate
regulation (C storage and GHG emissions) were generally improved by perennial crops (oil palm and
rubber), while indicators for macro invertebrate biodiversity and activity (0.73 ± 0.05) and soil macro
aggregation (0.76 ± 0.02) were highest within improved pastures. High variability within each system
indicates the potential to make improvements in fields with lowest indicator values, while differences
among systems suggest the potential to mitigate negative impacts by combining plots with contrasted
functions in a strategically designed landscape mosaic.
© 2014 Published by Elsevier B.V.

1. Introduction

The need to increase agricultural production for food and energy

∗ Corresponding author at: Institut de Recherche pour le Développement,
BIOEMCO, 32 rue H. Varagnat, 93143 BONDY Cedex, France.
E-mail address: Patrick.Lavelle@ird.fr (P. Lavelle).
1
Current address: University of California, Dept. of Plant Sciences, Davis, CA
95616, United States.
resources is driving agricultural frontiers into the last remaining
arable lands (Hubert et al., 2010). In Colombia, the Eastern Plains
(Llanos Orientales) are now being rapidly converted from semi-
natural savanna, dedicated largely to extensive cattle ranching and
low-input traditional agriculture, to highly intensified commercial
production of food (rice, soy bean, maize), biofuels (sugar cane and
oil palm) and rubber. It is estimated that over 50,000 ha has been

0167-8809/$ – see front matter © 2014 Published by Elsevier B.V.

http://dx.doi.org/10.1016/j.agee.2013.12.020
 P. Lavelle et al. / Agriculture, Ecosystems and Environment 185 (2014) 106–117
converted in the last two decades and recent trends show this agri-
cultural expansion to be accelerating (Romero Ruiz et al., 2012).
With economic development as the main driver of this growth, the
environmental implications for the Llanos and the entire Orinoco
River Basin are only beginning to be understood.
Representing a key hurdle to the agricultural intensification,
soils in the region are inherently acidic (pH currently in the range
of 3–5) and compact (bulk density in the range of 1.4–1.6 g cm−3 ).
Conversion to commercially viable agriculture thus requires the
formation of an arable soil layer via deep tillage to de-compact
soils, along with substantial applications of lime to increase soil
pH (Amézquita et al., 2004). Following this soil intervention, large
expanses of monoculture (up to several hundred hectares) are typi-
cally established, where chemical fertilizers are applied along with
a mixture of biological (e.g., Beauveria bassiana spores) and syn-
thetic pesticides, according to individual crop requirements. Soil
function and the provision of ecosystem services are thus dramati-
cally modified (Decaëns et al., 1994). However, the implications of
this abrupt management shift are likely to vary depending on the
cropping system that is implemented and the ecosystem service or
property being considered (Wall, 2012).
While there currently exist a clear intention on the part of the
Colombian government to ensure that development of the Llanos
is sustainable in social, economic and environmental dimensions
(Rippstein et al., 2001), similar dynamics that have played out
over the last 20 yr in the Brazilian Cerrado region (Goedert, 1989)
urge caution in this process. Development of the Cerrados clearly
achieved large gains in terms of productivity and economic yields,
but irreparable errors were also incurred in the process, leading
to extensive degradation of natural capital that should be avoided
wherever possible (Jepson, 2005; Guecker et al., 2009). The very
low initial quality of soils in the Llanos makes them particularly sus-
ceptible to erosion and biodiversity loss, while the dense network
of waterways and riparian forest traversing the region are likely
to face adverse effects associated with changes in water quality,
nutrient load, and movement – resulting from large scale imple-
mentation of intensive production systems (Sanchez and Salinas,
1983).
While soil and environmental degradation is likely to occur
in many cases, the enhancement of intrinsic soil properties and
associated increases in productivity may also improve soil qual-
ity and functioning via the promotion of biological activity and
biodiversity in soils (Decaëns et al., 1994), facilitation of below-
and aboveground C sequestration, and improvement of soil hydro-
logical functions due to improved soil structure (Amézquita et al.,
2004). Despite these potential benefits, a clear understanding of
the net impacts associated with land use conversion in the Llanos
is essential for guiding future development policy and land man-
agement decisions.
In order to address this need, we assessed the provision of soil-
based ecosystem services in four prominent and rapidly expanding
production systems in the Llanos: annual crops (maize, rice and
soybean), improved pastures, oil palm and rubber and compared
these with semi-natural savanna as a reference. Soils provide a
large number of important ecosystem services such as plant nutri-
ent provision, water storage and regulation, maintenance of soil
structure, and climate regulation, while conserving a very impor-
tant component of agro ecosystem biodiversity (i.e., soil macro
invertebrate communities) (Millennium Ecosystem Assessment,
2005; Wall, 2012). These services can be measured by a set of soil
parameters assembled in composite indicators of a specific service
(Velasquez et al., 2007a). We hypothesized that there would be
clear tradeoffs, such that each system would benefit at least one
ecosystem service relative to the natural savanna, but that the pro-
vision of other services would likely decline. We also sought to
identify shortcomings of current practices within each production
107
system that could be targeted for improvement in the development
of new management options.
2. Materials and methods
2.1. Site information and study design
The study region, in the Altillanura Plana of Colombia, extends
northeast from the Meta Department to the Venezuelan border
and is bounded to the north by the Andean Cordillera Oriental. At
roughly 200 m in elevation, climate is characterized by distinct wet
and dry seasons, with very little rainfall between December and
March and average annual temperatures around 26 ◦ C. Soils are
mainly Oxisols with low fertility and high acidity and Al saturation
(Lascano and Estrada, 1989; IGAC, 2004).
The study was conducted along a 200 km transect, running
East from Puerto Lopez towards Carimagua, paralleling the Meta
River to the north (Fig. 1). There exists a slight gradient in pre-
cipitation between Puerto Lopez (2700 mm yr−1 ) and Carimagua
(2300 mm yr−1 ) as well as a subtle gradient in soil texture, with
sand content higher in Puerto Lopez than in Carimagua; however,
with marked local variability. To be consistent with the objective of
the study of providing data relevant for the whole region of the Altil-
lanura, we choose 15 replicates for each system, distributed across
the entire region using a stratified approach, so that five fields of
each treatment were located within each of three areas along the
regional transect. Each field, in turn, was characterized by the same
complete set of parameters, replicated 3 times at 200 m intervals
inside the field, to provide a representative average measurement
of soil parameters in the plot with all points located at least 50 m
from field edges.
Although it was not possible to get clear information on
the age and history of the cultivated plots, some general infor-
mation could be collected. Humans have long impacted the
original savanna with a clear management intensity gradient
from Carimagua, where the most preserved savannas with rather
dense tree cover could be found, to Puerto Lopez where all trees
had been eliminated and grazing pressure was high. Improved
pastures were rather heterogeneous, since the oldest ones may
have been installed some 10–15 yr ago and are degraded with
relatively high densities of weeds and heavily compacted soils.
Transitory crops are always recently implemented systems since
cropping is usually maintained for a few cycles, during 2–4 yr
before perennial tree crops are installed. Rubber and oil palm had
been installed 3–10 yr prior to sampling in all cases. While these
systems are typically installed in fields following annual crops,
some rubber plots in Carimagua had been directly converted from
savanna.
2.2. Soil and ecosystem service assessment
Soil and macro fauna sampling was conducted in June and
July of 2011, during the rainy season. At each sampling point
we assessed soil chemical and physical characteristics, soil macro
invertebrate communities, C in plant aboveground biomass and
greenhouse gas (GHG) emissions. Soils were sampled at two depths
(0–10 cm and 10–20 cm) from a central monolith at each sampling
point (25 cm × 25 cm) after soil macro invertebrates were sorted
out.
2.3. Biodiversity
Macro invertebrates, considered an indicator of soil biodiversity,
were sampled using the TSBF methodology (Anderson and Ingram,
1993). Soil was extracted from a central 25 cm × 25 cm × 20 cm
monolith plus two other monoliths 25 cm × 25 cm × 10 cm located
108 P. Lavelle et al. / Agriculture, Ecosystems and Environment 185 (2014) 106–117
Fig. 1. Location of the 75 plots sampled between June and July, 2011, in the Meta Department, Colombia.
10 m N and S respectively from the central point. These samples
were hand-sorted in the field and macro fauna separated into 16
taxonomic groups, largely separated by order. Each plot was then
characterized using the sum of macro invertebrates found in the
three monoliths.
Nutrient provision services, or the ability of management
systems to support primary production, were evaluated using
standard analytical methods of 20 variables associated with soil fer-
tility (Anderson and Ingram, 1993), evaluated at both the 0–10 cm
and 10–20 cm depths. These variables included C and N contents,
cation exchange capacity (CEC), Al saturation, macro- and micronu-
trient concentrations (Ca, K, Mg, P Bray II, Al, B, Fe, Mn, Cu and Zn).
Soil pH was measured in a 2:1 water solution.
2.4. Soil hydrological services
A large set of soil physical properties was combined in a com-
posite indicator considered a reliable surrogate for soil hydrological
services. These comprise infiltration that avoids erosive surface
runoff, storage of water at different potentials for subsequent plant
use and prevention of inundations in low-lying areas. A set of 12
relevant variables were assessed: volumetric and gravimetric mois-
ture content, micro (<0.03 ␮), meso (0.03–3 ␮) and macro (>3 ␮)
porosity, plant available water retained at tensions between water
holding capacity (−0.1 MPa) and wilting point (−15 MPa), aggre-
gate stability, bulk density, resistance to vertical penetration and
shear strength resistance. All measurements were taken at 0–10
and 10–20 cm depths. Samples used for bulk density were removed
from the vertical walls of the central monolith excavated for soil
macro fauna sampling, and texture was measured on the same soil
sample used for chemical assessments.
Soil stability assessed by aggregate morphology provides an
integrative measure of soil biological activity over the past several
years and is an important determinant of the physical stabiliza-
tion of soil C, rooting potential, infiltration and aeration. Aggregate
morphology was evaluated using a method developed by Velasquez
et al. (2007b). Two small blocks 10 cm × 10 cm × 10 cm were taken
on each side of the central monolith and carefully placed into plas-
tic boxes for transport to CIAT. In the laboratory, these soil blocks
were gently separated into their aggregated components and clas-
sified as: biogenic, root or physical aggregates (according to their
origin and shape), non-macro aggregated soil (passing through a
5 mm sieve), stones and large organic particles (roots, litter or wood
pieces). Elements separated in this way were then air dried and
weighed.
Climate regulation, associated with soil processes and above-
ground vegetation was assessed through two components, C
storage in above- and belowground biomass and emissions of GHG
using static field chambers. The closed static chamber technique
measures emissions of green house gases (methane, nitrous oxide
and carbon dioxide) from the soil plant system. Proposed in 1981 by
Mosier and Hutchinson, it has been widely used since. Morris et al.
(2013) have shown that a set of discrete measurements spread over
a several week time period provide data sets that are comparable to
continuous measurements made by automatic systems. The great
spatial and temporal variability of emissions requires the use of var-
ious chambers and the uptake of 4–5 air samples taken at 5–10 min
intervals to check for non-linear gas fluxes in time (Rochette and
Eriksen-Hamel, 2008). Differences in plant cover associated with
land use affect microbial biomass and activity, soil C and N contents
and physical properties. These patterns, in turn, greatly affect GHG
fluxes, especially N2 O.
 P. Lavelle et al. / Agriculture, Ecosystems and Environment 185 (2014) 106–117 109

Fig. 2. Projection of chemical variables (a) and the 75 sampling points according to crop systems (b) in the plane formed by Factors 1 and 2 of PCA analysis. C, Ca, K, Mg. . .:
respective contents in different soil nutrients; Subscript number indicate soil layer (1 = −10 cm; 2 = 10–20 cm); CEC: cation exchange capacity; ECEC: effective cation exchange
capacity; Al Sat: saturation of the cation exchange capacity by Al cations, measured by two methods (1 and 2). (b) Letters indicate localization of the barycenter for each
system; ellipses show envelope for 75% points of a given category; T: Transitory crops, IP: Improved Pastures, R: Rubber plantations, NS: Natural Savanna, OP: Oil Palm
plantations. Ellipses show envelop for 75% of points from a given system. (p < 0.01: Monte Carlo permutation test on coordinates of the sampling points).

Nitrous oxide (N2 O), carbon dioxide (CO2 ) and methane (CH4 )
emissions from the sampling farms were measured monthly from
June to November of 2011 using static chamber technique in field
conditions (Chu et al., 2007). Three circular PVC collars were perma-
nently installed at each sampling point. Prior to each gas sampling,
cylindrical PVC chambers (0.03 m2 , 10 cm height) were clamped
and hermetically sealed to the collars. Air samples were then col-
lected from each chamber at 0, 15 and 30 min following placement
of the caps, using 20 mL disposable syringes fitted with plastic stop-
cocks (Cole Palmer Instruments Co.). Samples were analyzed for
N2 O and CH4 on a gas chromatograph equipped with an electron
capture detector (ECD) and Flame ionization detector (FID). Car-
bon dioxide was determined in an analyzer with infrared detection.
Changes in volumetric concentration of each gas was converted to
a mass flux by using the ideal gas law, taking into account recorded
changes in temperature within the chamber over the sampling
intervals. Fluxes of the three GHGs were then used to calculate
global warming potential (GWP) and expressed in CO2 equivalent
units (IPCC, 2007).
Aboveground biomass was calculated as the sum of herba-
ceous and tree components. Herbaceous biomass was cut on
50 cm × 50 cm areas at each point, dried and weighed and the C
concentration was estimated as 50% of the dry biomass. Carbon
contained in woody material of perennial crops and savanna trees
was evaluated according to Mac Dicken (1997), using tree circum-
ference and height (measured with a LaserAce hypsometer) along
with allometric equations developed for the region (Ibrahim et al.,
2007). Carbon storage in the upper 20 cm of soil was determined
based on the C concentration and soil bulk density measurement
described above.
2.5. Data analysis
Variables associated with nutrient provision services, soil phys-
ical and hydrological properties, aggregate morphology and soil
biodiversity were processed separately for each service following
the methodology adapted from Velasquez et al. (2007a) to create
a set of synthetic indicators that would capture the largest part of
variance expressed by the different variables. An initial principal
component analysis (PCA) allows for identification of the vari-
ables that best discriminate among the different plots and land use
types. Variables with significant contribution (>50% of the maxi-
mum value) to either of the first two principal component axes are
selected and their contribution to PCA axes 1 and 2 multiplied by
the overall variability explained by each PCA axis in order to gener-
ate a weight factor for each variable. Values for each variable were
then multiplied by their corresponding weight factor and summed
to generate a raw sub-indicator value using the following formula.
Ii1 = F1 × (˛I a + ˇI b + I c· · ·) + F2 × (˛II a + ˇII b + II c· · ·)
where Ii is the value of the indicator of service i (e.g.,. nutrient pro-
vision services) at point 1; F1 is the % of variance explained by PCA
axis 1 of the data set I; ˛I , ˇI and  I the respective contributions of
variables a, b and c to factor I and a, b and c the values of variables
measured at the point 1 considered. This value was then scaled to
a number ranging from 0.1 to 1.0 by a homothetic transformation,
for comparability across sub-indicators.
The general methodology used for climate regulation services
did not apply since clear internationally recognized summary vari-
ables (GWP and C storage) already exist. We therefore used primary
110 P. Lavelle et al. / Agriculture, Ecosystems and Environment 185 (2014) 106–117
Fig. 3. (a–d) Indicators of soil-based ecosystem services and soil quality provided among 5 production systems in the Altillanura plana region of Colombia. Error bars represent
the standard error of the mean. Different letters above bars indicate significant differences (p < 0.05).
data and generated two indicators, one of C storage in soils and
biomass (expressed as Mg C ha−1 ) and the other involving emis-
sions of GHGs (CO2 , CH4 and N2 O) expressed as a CO2 equivalent
flux. These values were also scaled to a 0.1–1.0 range of variation
and we used the average of the two sub-indicators to allow com-
parison of a general indicator of climate regulation with the other
4 indicators.
All analyses were conducted using the mean of the three samp-
ling points for each field. Multivariate PCA and coinertia analyses
and permutation Monte Carlo test to compare production sys-
tems were realized using the R environment and ade-4 library
(Thioulouse et al., 1997; R Development Core Team, 2004). Univari-
ate comparison of the synthetic indicators across cropping systems
with ANOVAs was carried out using JMP 9.0 software (SAS Institute,
2010). The assumptions of ANOVA (homoscedasticity and normal-
ity) were verified and log transformations were applied as needed.
3. Results
3.1. Nutrient provision services
Soils were relatively acidic with average values of 4.66 in
natural savannas and oil palm plantations to 5.03 in lime-amended
annual crops (Table 1). Fertilization and amendment of soils
had strong impacts on Al saturation that was reduced to 25.26%
on average in annual crops from an initial 79.23% in original
savannas, but still exhibited high values between 50 and 75%
in the other management systems. Soil management generally
increased C and N contents from 1.97% and 0.10%, respectively,
in the original savanna to maximum values of 2.72% and 0.14% in
improved pastures. Soil nutrient contents were largely influenced
by fertilization processes with average effective cation exchange
capacity increased from 2.41 g kg−1 in savanna to a maximum of
4.78 g kg−1 in annual crops, with particularly large increases in Ca,
Mg and available P contents (Table 1).
Since soil chemical fertility varied considerably, the 75 different
plots were clearly separated by PCA on the 40 variables describing
their respective chemical characteristics in 0–10 cm and 10–20 cm
soil layers (Fig. 2). The first principal components axis clearly
expressed a gradient of soil fertility: all but seven (Al total content
at 0–10 cm and Al saturations 1 and 2 at 0–10 and 10–20 cm, Fe
at 0–10 and 10–20 cm depth) soil variables projected on the same
side of the first factorial axis (36.6% explained variance), thus clearly
opposing soils rich in nutrients and with high C and N, to poor soils
with low organic matter and nutrient content (Fig. 2a). The second
axis (15.5% of explained variance) was associated with soil acidity
and opposed soils with higher pH values and Ca and Mg contents,
to acid soils with high Al saturation.
Production systems were aligned along axis 1 and separa-
tion was significant (29.3% variance observed, p < 0.001; Fig. 2b).
Semi-natural savanna and palm tree plantations were located at
one end, annual cropping systems at the opposite extreme, with
improved pastures and rubber plantations in the middle. Axis 2
rather exhibited variability inside systems. The indicator formula
 P. Lavelle et al. / Agriculture, Ecosystems and Environment 185 (2014) 106–117
Fig. 4. Correlation circle of soil macro fauna variables with factors 1 and 2 (left) and projection of sample points in the plane defined by factors 1 and 2 (right) of a PCA
analysis of data from the 5 production systems analyzed in the Altillanura plana region of Colombia. EWM: earthworms, P: Improved pastures, SN: Natural savanna, PA: Oil
Palm plantations, C: Rubber plantations, T: Transitory crops.
was calculated with 29 of the 40 initial variables that had respec-
tive weights larger than 50% of the highest value, following the
procedure recommended by Velasquez et al. (2007a). Differences
between production systems for the soil chemical fertility indicator
were significant (ANOVA test: p < 0.01) with lowest average values
observed in semi-natural savanna (0.31 ± 0.04) and oil palm plan-
tations (0.32 ± 0.02) and highest in annual crops (0.78 ± 0.03), with
improved pastures and rubber plantations having intermediate val-
ues (Fig. 3a).
3.2. Soil hydrological functions
Soils exhibited rather important variations in texture, with sand
content ranging from 21 to 81% (mean: 47.2%; Table 2), while bulk
density was high on average (1.44), varying between 1.1 and 1.67
(both soybean fields with highly contrasted conditions). Available
gravimetric water was generally low, between 1.9 and 11.0% (aver-
age: 5.7%) and mean diameter values for stable aggregates varied
from 1.8 to 6.1 (average: 4.2 mm, Table 2).
The indicator was constructed using 11 of the 12 variables char-
acterizing hydrologic properties and suggested higher values for
perennial crops and natural savannas, but the ANOVA test was not
significant (p > 0.05; Fig. 3b).
3.3. Soil biological function and diversity
Soil macro invertebrate communities varied widely with land
use, ranging from a minimum of 26.7 ind. m−2 (under rice) to
9504 ind. m−2 (in improved pasture), with an overall average of
2227. Termites were by far the most abundant group (71.8%), fol-
lowed by ants (16.6%), earthworms (2.8%) and Coleoptera (2.6%).
Improved pastures (3793 ± 761 m−2 ) had the largest communities,
followed by oil palm plantations (2394 ± 491 m−2 ), native savanna
(2225 ± 590 m−2 ) rubber plantations (1872 ± 561 m−2 ) and annual
crops (619 ± 264 m−2 ; Table 3).
Earthworm communities exhibited higher densities in savanna
(60.1 ± 3.0 m−2 ) than in all systems (Table 3), except for improved
pastures (173.9 ± 8.6 m−2 ), where densities were increased by
almost a factor of three. They were mostly comprised of endogeic
earthworms (92.2%). Meanwhile, termite abundance was highest
in improved pastures (1283 ± 81.3 m−2 ) and lowest in the under
annual crops (211 ± 35 m−2 ; Table 3). Contrary to the general trend
111
observed in termites and earthworms, the other important ecosys-
tem engineers as defined by Jones et al. (1994); ant abundance was
highest in the semi-natural savanna (724 ± 36 m−2 ). Taxonomic
richness also decreased from the more natural to more disturbed
areas since soil nesting species dominant in savanna and pasture
soils are the most sensitive to disturbances.
The indicator of macro invertebrate abundance and diversity
significantly separated systems (p < 0.001) with highest values
in improved pastures (0.73 ± 0.05), followed by native savannas
(0.58 ± 0.04); oil palm (0.57 ± 0.03) and rubber (0.52 ± 0.03), all far
above annual crops (0.29 ± 0.04; Fig. 3c).
Principal component analysis of the data matrix (comprised of
abundance for 7 large taxonomic units and taxonomic richness,
sum of invertebrates collected at each of the 75 plots) confirmed the
trends expressed above and clearly ranked sites along axis 1 (43.8%
of variance explained; Fig. 4) according to the abundance of all the
invertebrate groups, in the order: Improved pastures (IP), natural
savanna (NS), oil palm plantations (OP), rubber plantations (R) and
annual crops (T). Axis 2 opposed sites with large densities of Myri-
apoda (annual crops with large Polydesmid populations) to natural
savannas, improved pastures and oil palm plantations respectively,
characterized by high populations of Coleoptera and social insects.
Production systems explained 25.7% of variance according to the
permutation test (p < 0.001).
3.4. Soil macro aggregation
On average, only 37.9% of the soil volume was not macro-
aggregated, with biogenic aggregates contributing 35.8% of the
total soil mass and physical aggregates comprising 25.1%. Impor-
tant differences were suggested in macro fauna associated biogenic
aggregates, with this fraction representing only 14.3% of the soil
under annual crops and oil palm plantations, while savanna and
improved pastures possessed much larger percentages of the whole
soil as biogenic aggregates (48.3 and 56.6%; respectively).
Natural savannas, improved pastures and rubber plantations
respectively, with high amounts of biogenic aggregates in soils,
were opposed along axis 1 (31.4% explained variance) of PCA, to
annual crops and palm tree plantations, with a predominance of
physical aggregates and non-macro aggregated soil (figure not
shown). Axis 2 (23.2%) separated plots with high amounts of
stones and non-aggregated soil. This effect was independent from
systems and likely linked to local soil conditions. The permutation
112 P. Lavelle et al. / Agriculture, Ecosystems and Environment 185 (2014) 106–117

Fig. 5. Indicators of C storage (a) and green house gases emissions (b) in the 5 production systems analyzed in the Altillanura plana region of Colombia. Error bars represent
the standard error of the mean. Different letters above bars indicate significant differences (p < 0.05).

test showed a clear effect (32.4% variance explained; p < 0.01) of

production systems on soil morphology.
The indicator was constructed using four of the six measured
variables (physical, biogenic and root aggregates, plus non aggre-
gated soil) and exhibited significant differences among the five
production systems. Improved pastures (0.76 ± 0.02) and native
savannas (0.63 ± 0.07) had the highest average values, rubber
plantations intermediate values (0.59 ± 0.03) and annual crops
(0.36 ± 0.04) and oil palm (0.30 ± 0.03) the lowest values (Fig. 5a).

3.5. Climate regulation services

Carbon measured in the five systems was predominantly

stored as soil organic matter. According to the systems, C
stored in the upper 20 cm of soil varied relatively little, from
52.1 ± 2.6 Mg ha−1 in rubber plantations to 69.7 ± 3.2 Mg ha−1
in improved pastures (ANOVA test p < 0.01). As expected, C
storage in aboveground plant biomass exhibited much greater
differences among systems, with lowest values in annual crops
(1.7 ± 0.3 Mg ha−1 ) and grasslands and highest in the oil palm
(35.3 ± 7.0 Mg ha−1 ) and rubber (19.3 ± 7.8 Mg ha−1 ) plantations
(Fig. 5a). In total (sum of above- and belowground C), oil
palm plantations (88.9 ± 7.8 Mg ha−1 ) had significantly higher val-
ues than native savannas (58.6 ± 2.6 Mg ha−1 ) and annual crops
Fig. 6. Coefficient of matrix correlation (Rv ) among tables of data for the differ-
(62.0 ± 2.5 Mg ha−1 ), while improved pastures and rubber planta-
ent indicators of ecosystem services, and associated p values (*p < 0.05; **p < 0.01;
tions, had intermediate values (Fig. 5a). ***p < 0.001).
Emissions of GHGs varied according to the production sys-
tems considered and also among gases. N2 O comprised 71.5% of
total GWP, CO2 (27.2%) and CH4 (1.3%). With the highest observed values for all the other indicators (i.e., macro invertebrate commu-
N2 O emissions (871.4 ± 233.2 g equ. CO2 m−2 yr−1 ), annual crops nities, C storage, soil aggregation or hydrological properties). Axis 2
had the highest GWP (1071.3) emissions, while oil palm plan- explained a similar amount of variance to F1 (24.0%) and contrasted
tations had the lowest (544.8 ± 233.2 g equ. CO2 m−2 yr−1 ). These improved pastures (displaying optimal morphological properties)
differences, however, were not significant (Fig. 5b). with oil palm plantations, demonstrating the best soil physical
qualities. Graphic representation of indicators of soil ecosystem
3.6. Covariations among indicators of ecosystem services services showed that all production systems have at least one indi-
cator that is substantially improved over the semi-natural savanna.
Coinertia analysis among data matrix of each indicator demon-
strated significant covariations for all pairs of data sets, although 4. Discussion
with relatively low values for the respective matricial correlation
coefficient (0.098–0.257; Fig. 6). Principal component analysis of Soils of the Altillanura region demonstrated poor fertility as
indicators discussed above showed a significant effect of produc- expected (Amézquita et al., 2004). In semi-natural savanna, soils
tion systems (34.3% variance explained; p < 0.001) and allowed were generally acidic and compacted with high Al saturation and
to identify the impact of each system on soil function and envi- relatively low organic matter storage in the upper 20 cm of the
ronmental variables (Fig. 7). Axis 1 (27.7% of explained variance) soil profile (Sanchez and Salinas, 1983). This result agrees with
opposed annual crops, with high chemical fertility and GHG emis- previous studies conducted in the 90s aimed at improving soil
sions, with all the other systems, which generally expressed higher conditions (Amézquita and Londoño, 1997; Amézquita, 1998).
 P. Lavelle et al. / Agriculture, Ecosystems and Environment 185 (2014) 106–117 113

Hydrological
services

GHG
Emissions
C storage

Macrofauna

Soil Chemical
macroaggregaon Ferlity OP

R
NS

IP

Fig. 7. Correlation circle of indicators with factors PCA 1 and 2 (upper left), and projection of individual plots of each production system on the F1 /F2 plane defined by PCA
on indicators.

Table 1
Chemical properties (mean and range) in the upper 10 cm of soil in five production systems of the Llanos Orientales region of Colombia, sampled in June and July, 2011.

Annual crops Natural savanna Improved pastures Oil Palm plantations Rubber plantations

Mean Range Mean Range Mean Range Mean Range Mean Range

pH 5.03 (4.35–6.30) 4.68 (4.14–5.27) 4.78 (4.14–5.64) 4.64 (4.03–5.50) 4.91 (3.86–6.68)
MO g kg−1 4.27 (2.42–7.17) 3.39 (1.13–5.6) 4.69 (2.22–6.72) 3.65 (1.71–6.60) 3.46 (1.55–5.22)
C g kg−1 2.48 (1.41–4.17) 1.97 (0.66–3.25) 2.72 (1.29–3.90) 2.12 (0.99–3.84) 2.01 (0.90–3.03)
N g kg−1 0.12 (0.06–0.19) 0.10 (0.05–0.16) 0.14 (0.07–0.20) 0.11 (0.06–0.17) 0.11 (0.08–0.17)
C:N 20.98 (13.7–55.28) 19.77 (12.82–24.42) 20.39 (17.19–24.16) 20.47 (17.61–35.72) 19.69 (12.59–23.36)
P Bray II mg kg−1 27.85 (0.86–113.01) 3.00 (0.27–44.26) 4.50 (0.62–30.79) 4.73 (0.61–57.72) 10.32 (0.49–143.37)
K mg.Kg−1 0.21 (0.03–0.45) 0.06 (0.02–0.16) 0.09 (0.02–0.30) 0.08 (0.02–0.31) 0.08 (0.01–0.26)
Ca mg kg−1 2.61 (0.08–5.85) 0.36 (0.07–3.02) 0.75 (0.03–3.94) 0.38 (0.07–2.18) 1.11 (0.10–3.79)
Mg mg.Kg−1 0.97 (0.04–2.03) 0.14 (0.03–0.85) 0.30 (0.03–1.41) 0.16 (0.04–0.83) 0.38 (0.07–1.38)
AI mg kg−1 0.99 (0–3.25) 1.86 (0.3–4.2) 1.91 (0.00–3.60) 2.00 (0.00–4.20) 1.48 (0–4.00)
CIC cmol kg−1 11.12 (4.4–19.2) 8.04 (2.8–16.1) 10.48 (3.30–19.70) 8.03 (1.70–13.00) 8.97 (2.89–14.70)
CICE cmol kg−1 4.78 (1.47–8.09) 2.41 (0.84–6.38) 3.06 (0.96–5.38) 2.62 (0.72–4.44) 3.04 (1.12–6.24)
Al Sat1% 25.26 (0–92.18) 79.23 (12.11–94.88) 65.82 (0.00–92.86) 73.37 (0.00–94.55) 50.23 (0–92.23)
Al Sat2% 9.45 (0–34.00) 24.86 (3.54–38.71) 19.31 (0.00–37.74) 28.76 (0.00–200) 16.85 (0–62.22)
S mg kg−1 21.48 (8.06–49.82) 14.94 (0–27.84) 15.79 (7.09–29.37) 11.64 (0.00–34.57 12.68 (1.11–29.89)
B mg kg−1 0.40 (0.1–0.69) 0.25 (0.02–0.51) 0.31 (0.12–0.46) 0.29 0.07–0.64) 0.30 (0.03–0.54)
Fe mg kg−1 54.14 (8.02–395.26) 44.25 (18.4–336.32) 62.39 (15.03–227.27) 46.82 (18.9–241.7) 73.88 (10.52–528.45)
Mn mg kg−1 6.28 (0.69–27.22) 1.72 (0.45–8.17) 4.57 (0.63–23.36) 2.22 (0.32–8.57) 2.96 (0.55–12.8)
Cu mg kg−1 0.67 (0.13–1.52) 0.34 (0.06–1.05) 0.64 (0.24–2.34) 0.42 (0.09–1.68) 0.35 (0.09–0.84)
Zn mg kg−1 3.13 (0.35–10.04) 0.86 (0.19–12.63) 1.42 (0.26–6.43) 0.99 (0.31–6.01) 0.87 (0.26–3.50)

Table 2
Physical properties (mean and range) in the upper 10 cm of soil five production systems of the Llanos Orientales region of Colombia, sampled in June and July, 2011.

Annual crops Natural savanna Improved pastures Oil Palm plantations Rubber plantations

Mean Range Mean Range Mean Range Mean Range Mean Range

Soil moisture (g 100 g−1 ) 35.09 (25.33–48.00) 31.32 (12.67–42.33) 34.93 (30.67–40.67) 34.93 (30.67–40.67) 34.77 (23.33–44.33)
Soil moisture (cm3 100 cm−3 ) 50.09 (30.00–76.67) 46.04 (20–60) 50.2 (34.67–58.00) 50.2 (34.67–58.00) 47.23 (34–58.00)
Bulk Density 1.42 (1.09–1.67) 1.49 (1.26–1.66) 1.44 (1.11–1.63) 1.44 (1.11–1.63) 1.37 (1.24–1.57)
(g cm−3 )
Available water % 5.07 (3.60–8.44) 5.28 (1.92–7.15) 4.93 (3.05–7.24) 4.93 (3.05–7.24) 6.45 (3.00–8.89)
Macroporosity % 8,00 (3.92–16.77) 8.11 (3.09–15.63) 6.29 (3.36–11.68) 6.29 (3.36–11.68) 8.9 (5.12–15.31)
Mesoporosity % 7.74 (4.74–17.71) 8.44 (3.15–13.65) 6.76 (4.22–10.92) 6.76 (4.22–10.92) 9,00 (3.76–12.64)
Microporosity % 32.19 (14.94–43.09) 30.94 (15.39–38.67) 33.75 (23.3–40.82) 33.75 (23.3–40.82) 31.65 (23.5–42.71)
Tot. Porosity % 47.96 (30.00–59.33) 47.5 (39.67–57.00) 46.87 (38.33–55.0) 46.87 (38.33–55.00) 49.56 (41.00–56.00)
Mean Aggr. Diam. (mm) 4.44 (3.03–5.63) 4.2 (2.62–5.41) 4.58 (2.80–6.05) 4.58 (2.8–6.05) 4.57 (2.75–6.03)
Sand % 39.76 (28.83–58.83) 49.85 (21.5–81.33) 45.51 (30.79–63.07) 45.51 (30.79–63.07) 48.41 (23.50–72.29)
Silt % 32.65 (20.00–46.00) 28.49 (11.33–45.21) 31.63 (20.43–49.38) 31.63 (20.43–49.38) 30.2 (13.87–49.33)
114 P. Lavelle et al. / Agriculture, Ecosystems and Environment 185 (2014) 106–117

Table 3
Macro invertebrate communities (mean and range) in soil (0–20 cm) of five production systems of the Llanos Orientales region of Colombia, sampled in June and July, 2011.

Annual crops Natural savanna Improved pastures Oil Palm plantations Rubber plantations

Mean Range Mean Range Mean Range Mean Range Mean Range

Endogeic earthworms 25.96 (0–101) 56.90 (0–192) 156.09 (0–507) 35.91 (0–85) 40.18 (0–75)
(ind. m−2 )
Epigeic earthworms (ind. m−2 ) 1.42 (0–10.7) 3.20 (0–21.3) 1.78 (0–69) 1.42 (0–11) 2.49 (0–27)
Termites (ind. m−2 ) 211.20 (0–2800) 1282.00 (5–4661) 2939.00 (133–7856) 2022.00 (59–5989) 1540.00 (0–6992)
Ants (ind. m−2 ) 271.64 (0–2325) 723.56 (5–1888) 411.38 (43–869) 247.47 (11–704) 196.98 (0–1136)
Coleoptera (ind. m−2 ) 25.60 (0–187) 79.29 (5–219) 107.73 (21–352) 45.51 (11–133) 29.16 (5–59)
Myriapoda (ind. m−2 ) 32.36 (0–117) 9.24 (0–43) 24.53 (0–117) 16.00 (0–43) 18.13 (0–75)
Other litter invert. (ind. m−2 ) 50.49 (0–181) 70.40 (5–229) 136.18 (11–635) 25.96 (5–80) 45.51 (0–165)
Taxon. Richness 7.30 (2–11) 8.90 (6–15) 10.70 (7–15) 8.50 (5–12) 8.60 (6–13)

Table 4
Macroaggregates and other components in the upper 10 cm of soil for five production systems of the Llanos Orientales region of Colombia, sampled in June and July, 2011.

Annual crops Natural savanna Improved pastures Oil Palm plantations Rubber plantations

Mean Range Mean Range Mean Range Mean Range Mean Range

Physical macroaggregates (% dry weight) 49.31 (299–695) 9.85 (51–146) 12.78 (53.8–183) 40.05 (189–629) 15.26 (75–337)
Root macroaggregates (% dry weight) 0.24 (0–15.9) 0.15 (0–3.0) 0.26 (1.1–4.4) 0.12 (0–2.3) 0.12 (0–5.5)
Macrofaunal macroaggregates (% dry weight) 13.91 (59.7–476) 48.29 (91–779) 56.57 (467–772) 13.36 (43.7–250) 44.25 (47–633)
Non macro aggregated soil (% dry weight) 35.75 (105–479) 40.38 (226–861) 29.52 (141–456) 45.27 (214–774) 39.64 (188–565)
Plant Material (% dry weight) 0.70 (2.9–22.3) 0.68 (3.5–24.2) 0.86 (3.4–12.9) 1.20 (3.8–21.7) 0.74 (2.8–20.5)
Stones (% dry weight) 0.09 (0–12.9 0.63 (0–84) 0.00 (0–0) 0.00 (0–0) 0.00 (0–0)

While semi-natural savanna can have relatively abundant tree
cover and are not always so unproductive (Medina et al., 1978),
most savanna soils considered in this study have been impover-
ished by decades of extensive grazing and dry season fires (Medina
and Silva, 1990). Better preserved savannas, with rather dense
tree cover found in the most remote sites near Carimagua actually
exhibit much better conditions as they generally correspond to the
best values in the ranges of variables shown in Tables 1–5. Permu-
tation test on the chemical data set comparing the three regions
(Puerto Lopez, Puerto Gaitan and Carimagua) (not shown here)
significantly separates along axis 1 Carimagua sites from the other
ones. Particularly striking is that bulk density exceeds 1.6 g cm−3
in the upper 0–10 cm layer for some soils under semi-natural
savanna and other systems. This is likely the combined result of
fine texture, compaction by cattle and/or restricted activity of
large soil invertebrates. In this context, soil invertebrate ecosystem
engineers (termites, earthworms and ants) have been shown to
be major builders of soil macro porosity, particularly large anecic
earthworms found in the Carimagua area (Decaëns et al., 1999;
Decaëns et al., 2001), suggesting that restoration actions should
seek to promote their activities (Jimenez and Thomas, 2001).
Transformation of this soil for intensive farming purposes is
currently accomplished through the initial creation of an arable
layer (Amézquita et al., 2004). This practice consists of incor-
porating lime (3–6 Mg ha−1 ) to a depth of at least 30 cm with
deep tillage and fertilizer application. Annual crops are typically
planted during the first one or two seasons to take advantage of
the better-aerated soil and optimal chemical conditions, and are
often then followed by improved pastures and/or perennial crops
that benefit from residual nutrients and acidity reduction.
Indicators of the soil-based ecosystem services exhibited sig-
nificant covariations in all but one case, although with relatively
low (0.10–0.26) matrix correlation coefficients. This very important
result suggests that these services are at least marginally inter-
dependent and that any positive or negative effect on one of the
services is likely to be reflected in the others. The largest covariation
was observed among soil chemical fertility variables and physical
variables (0.26), soil macro aggregation pattern (0.21) and climate
regulation variables (0.18), suggesting that management of chem-
ical fertility is a major driver of soil processes in the region.
Our results suggest that chemical fertility is by far the best in
annual cropping systems, especially in the upper 0–10 cm soil layer,
with remarkably high contents of base cations (CEC increased from
2.41 mg kg−1 in natural savannah to 4.78 on average in the annual
cropping systems), while also demonstrating high C and N, and low
Al saturation (decreasing from 79.2% in natural savanna to 25.1%
with annual crops). To our surprise, pH was only slightly increased
in the upper 10 cm (4.68–5.03 on average) in annual crops, in com-
parison with other systems, and differences in acidity (associated
with high Al saturation of the soil exchange complex) only sepa-
rated annual crops and rubber plantations from the other systems
along axis 2 of the PCA analysis (15.6% of the explained variance).
Most variations observed in the upper 10 cm were dramatically
reduced in the 10–20 cm soil layer, showing that soil improvement

Table 5
Carbon storage in soil, above ground biomass and green house gas emissions by soils (mean and SE) of five production systems of the Llanos Orientales region, Colombia,
samples between July and December, 2011.

Annual Crops Natural savannah Improved pastures Oil Palm plantations Rubber plantations

Mean Range Mean Range Mean Range Mean Range Mean Range

C in biomass (Mg C ha−1 ) 1.74 (0.47–4.49) 2.50 (0.63–4.13) 2.57 (1.15–3.95) 35.30 (1.5–113.3) 19.28 (0.21–101.3)
Soil C (Mg C ha−1 ) 60.29 (30.7–74.5) 52.02 (5.45–68.5) 69.80 (44.3–92.7) 53.56 (29.8–64.8) 52.11 (31.9–65.7)
CO2 (kg m−2 yr−1 ) 0.20 (0.14–0.36) 0.15158 (0.03–0.26) 0.27053 (0.15–0.44) 0.20247 (0.11–0.37) 0.25 (0.11–0.52)
CH4 (mg m−2 yr−1 ) −22.92 (−529–428) 150.945 (−303–1547) 325.027 (−108–1565) 168.437 (−379–1120) 161.25 (−274–904)
CH4 equ. CO2 (kg/m2 yr−1 ) 0.00 (−0.04–0.03) 0.0109 (−0.02–0.11) 0.0234 (−0.01–0.11) 0.0121 (−0.03–0.01) 0.01 (−0.02–0.07)
N2 O (mg m−2 yr−1 ) 3015.36 (52–11768) 2096.93 (113–8414) 1441.09 (54.5–5232) 1142.52 (13.7–446.6) 1998.85 (476–6580)
N2 O equ. CO2 (kg m−2 yr−1 ) 0.87 (0.02–3.40) 0.6060 (0.03–2.43) 0.4165 (0.016–1.51) 0.3302 (0.004–0.77) 0.58 (0.14–1.90)
 P. Lavelle et al. / Agriculture, Ecosystems and Environment 185 (2014) 106–117
was only sustained in the upper 10 cm. Soil physical improvement
provided by deep tillage previous to the crop establishment was not
observed in our plots which suggests that improvement of physi-
cal characteristics, considered a necessary condition to implement
annual cropping systems (Amézquita et al., 2004), may be short-
lived within these production systems if no further intervention
occurs. We also note that indicators of other soil ecosystem ser-
vices, biodiversity (macro fauna communities index), soil stability
provided by macro aggregation, and climate regulation services
through C storage and control of GHG emissions, were lowest under
annual cropping systems.
The potential of improved pastures for enhancing soil macro
invertebrate communities (Decaëns et al., 1994) was clearly con-
firmed in this study. Increased C inputs from large roots and above
ground biomass likely provided better quality food as well as much
higher organic matter inputs. Earthworm densities increased three
fold from 56.9 to 156.1 ind. m−2 while termite densities more than
doubled from 1282 in semi-natural savanna to 2939 ind. m−2 under
improved pastures. Other groups, with the exception of ants, also
demonstrated generally higher densities under improved pastures
(Table 3). Taxonomic diversity also appeared to be higher, with the
average number of orders found at each sampling point increas-
ing from 8.9 to 10.7 in savanna vs. improved pastures, respectively.
Along with enhanced activities of the major soil ecosystem engi-
neers, we observed a 28.3% increase in the accumulation of biogenic
aggregates produced by macro fauna (Velasquez et al., 2007a,
2012), a 26.7% increase in physical aggregates and a resulting 28.3%
decrease in the non-aggregated soil fraction. At the same time, the
indicator for nutrient provision services (chemical fertility) was
57.6% higher than in the original savanna. While the indicator for
hydrological functions decreased from 0.43 ± 0.06 to 0.34 ± 0.04
(Fig. 2) on average under improved pastures, the combined climate
regulation index was the highest of all five systems with an aver-
age value of 0.55 (±0.04) much higher than recorded in the original
savanna (0. 34 ± 0.04; data not shown).
Perennial crops (palm and rubber) presented rather high values
for all indicators, and demonstrated the highest values for hydro-
logical functions (although differences were non-significant) and C
storage. The accumulation of C in aboveground biomass led to oil
palm plantations having the highest C storage (35.3 ± 7.0 t ha−1 ),
although the combined climate regulation indicator was second
to improved pastures as a result of the low GHG emissions in
these modified grasslands. The environmental impact of oil palm
plantations has been addressed in a rather large number of pub-
lications (Comte et al., 2012; Obidzinski et al., 2012; Smith et al.,
2012; Reijnders and Huijbregts, 2008) and our indicators need to
be assessed in a larger number of sites to reach a definitive con-
clusion on the overall impact of these systems. It is also important
to point out that the majority of the plantations considered in this
study were relatively young (<5 yr since implementation) and that
C benefits measured here for oil palm or rubber plantations are
likely to increase, but are also highly variable (Fig. 5a). Thus, uncer-
tainty in the net ecosystem C balance in these systems is great
(Ziegler et al., 2012). We therefore suggest that the synthetic indi-
cators developed here described a situation that may be largely
influenced by previous land use. Monitoring plantations from the
early stages to more mature perennial production systems would
provide a clearer view of the overall C balance and contributions
to ecosystem services over time. Previous studies have shown that
aged rubber plantations may lose high amounts of belowground
C, followed by significant decreases in soil macro fauna abundance
and diversity as plantations age (Gilot et al., 1995).
Overall, changes in soil chemical parameters following the initial
creation of an arable layer at all sites drastically improved concen-
trations and availability of P, K, Ca and Mg, while CEC was more than
doubled and average Al saturation reduced from ca. 80% in savannas
115
to 25% in annual crops (Table 1). Surprisingly, the changes observed
for pH, N and C contents were much less dramatic. Physical param-
eters in the upper 0–10 cm soil layer that determine hydrological
functions suggested some changes, although no significant differ-
ences were observed among systems. This result suggests that local
variability in soil texture and differences in the implementation of
mechanical activities when creating the arable layer can play an
important role in determining soil water dynamics.
The greatest differences across land uses were observed in
macro invertebrate communities and soil macro aggregation pat-
terns. Macro invertebrate communities indeed are highly sensitive
and quickly respond to subtle changes in resource availability and
habitat conditions, as is confirmed by abundant past literature
(Lavelle and Pashanasi, 1989; Decaëns et al., 1994; Barros et al.,
2002; Rousseau et al., 2013). Modification of macro invertebrate
communities, especially of soil ecosystem engineers that build and
shape the habitat in the upper 10–30 cm of soil, result in observable
changes in soil macro aggregation and macro porosity. More soil is
converted into biogenic aggregates (Lavelle et al., 2006; Velasquez
et al., 2012) and denser networks of galleries and other macro pores
are formed (Hallaire et al., 2000). These modifications often result
in long-term improvements to water infiltration and changes in
water retention patterns and can produce emergent effects at larger
scales (Lavelle et al., 2006). These changes, however, may take a
long time to become evident and translate into significant modifica-
tions of soil physical parameters. Alterations to chemical properties
generally occur at even greater time scales, except when massive
additions of lime and fertilizer generate an immediate change that
can often have persistent residual effects. For these reasons, pat-
terns observed in this preliminary examination of soil ecosystem
services in the region will need to be monitored over time to iden-
tify a clear trend and provide more conclusive information on the
respective long-term impacts of management. In any case, these
results confirm that soil macro invertebrate communities and mor-
phological analyses are highly sensitive early indicators of change
(Velasquez et al., 2012).
Along the same line, a significant proportion of the variance
among systems that is not explained by differences in the produc-
tion system is probably due to differences in past management,
previous to system installation. The transition phase between the
initial degraded savanna and the newly intensified agro ecosys-
tem is critical since conditions inherited from the original state
(organic matter and nutrient concentrations, soil aggregation, bio-
diversity) may drive essential soil processes towards divergent
pathways according to their characteristics. Holling (2001) states
that conditions of connectedness and potential at the onset of a
new adaptive cycle, determine the trajectory that the ecosystem
will follow as it progressively shifts from the “release” to the “reor-
ganization” and “exploitation” phases of the cycle. This means that
biodiversity and biogeochemical cycles inherited from the origi-
nal semi-natural savanna, that determine “connectedness” and the
“potential” (here expressed as organic matter, nutrient reserves
and, possibly, accumulated soil macro aggregation), are essential
features to understand the state of the system at the time we con-
ducted the diagnostic, and for understanding current and future
trajectories of ecosystem change.
Organization of the landscape and proximity to natural sys-
tems may be a third determinant of the observed variation (Lovell
and Johnston, 2009). An interesting outcome of this study is the
difference in provision of soil based-ecosystem services by differ-
ent production systems. Annual crops enhance the nutrient supply
potential of soils and represent an attractive option to achieve fast
economic return which may be needed to compensate the cost
of creating an arable layer (Amézquita et al., 2004). On the other
hand, these systems suggest large negative impacts on soil macro
invertebrate communities and other soil ecosystem properties that
116 P. Lavelle et al. / Agriculture, Ecosystems and Environment 185 (2014) 106–117
could be mitigated if favorable systems adjacent to these field plots
could serve as colonization sources. Alternation of complemen-
tary systems, in time by rotations or in space via strategic spatial
arrangement of plots would allow interactions and increase con-
nectedness at landscape scale. This would allow the whole matrix
of plots dedicated to different uses for conserving soil capital and
its capacity to provide ecosystem services.
Beyond local landscape construction, limits to large-scale land
conversion should be set taking into consideration biodiversity
retention, ecosystem engineer promotion and waterway protec-
tion in relation to long-term landscape health. Considering the
organization of the agricultural territory at landscape scale is
of utmost importance when considering the fate of the dense
network of gallery forests that cover roughly 20% of the area
and of the streams and other water bodies. Lovell and Johnston
(2009) state that “Although the conventional approach to land-
scape ecology is based on a model that assumes poor ecological
quality in the human-dominated matrix, a review of recent liter-
ature reveals important opportunities to improve the quality of
the landscape matrix by increasing spatial heterogeneity through
the addition of semi-natural landscape elements designed to pro-
vide multiple ecosystem services. Taken alone, these individual
elements might not appear to have a large impact on the environ-
ment, but when considered together within the entire landscape,
the contribution could be significant, particularly when these
elements are intentionally designed to improve landscape perfor-
mance”.
In the meantime, accurate monitoring of soil quality and pro-
vision of ecosystem services should be developed to detect soil
degradation and prevent irreversible impacts. Soils of the Llanos
region are heavily compacted (apparent density around 1.5–1.6),
with low hydraulic conductivity and very limited porosity to retain
water available to plants (in the range 4–6% on average). Prac-
tices that would deteriorate even more this situation would likely
increase flooding and surface runoff with associated increased risk
of soil erosion and transfer of nutrients from surface applied fertil-
izers to rivers. At a larger scale, this could yield severe implications
for the larger Orinoco River Basin (i.e., degradation of water qual-
ity, eutrophication, and facilitation of dissolved organic C fluxes
to the atmosphere). Applying the same sort of indicators that we
present in this study may carry out diagnostics of soil quality and
other soil ecosystem services. The identification of significant vs.
non-impacted variables made in this study will permit the appli-
cation of protocols with a significant reduction in the number of
variables measured, but with only minimal losses to sensitivity and
the information obtained. Furthermore, we recommend perform-
ing analyses of ecosystem services at the landscape scale and over
time, in order to increase the understanding of determinants of ES
and allow designing ecoefficient agricultural landscapes.
Acknowledgements
First, we would like to thank the farmers involved in this study
that allowed us to conduct research on their land. We would also
appreciate the contributions of Arbey Alvarez, Mercedes Castaneda,
Carolina Quintero and others who helped in the field and labora-
tory, as well as Jorge Lozano and others in CORPOICA who provided
important logistical support. We also thank Silvia Elena Castano
and Carlos Nagles for providing the map. The Colombian Ministry
of Agriculture funded this research.
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